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Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms

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Abstract

Plants growing under field conditions are constantly exposed, either simultaneously or sequentially, to more than one abiotic stress factor. Plants have evolved sophisticated sensory systems to perceive a number of stress signals that allow them to activate the most adequate response to grow and survive in a given environment. Recently, cross-stress tolerance (i.e. tolerance to a second, strong stress after a different type of mild primary stress) has gained attention as a potential means of producing stress-resistant crops to aid with global food security. Heat or cold priming-induced cross-tolerance is very common in plants and often results from the synergistic co-activation of multiple stress signalling pathways, which involve reactive nitrogen species (RNS), reactive oxygen species (ROS), reactive carbonyl species (RCS), plant hormones and transcription factors. Recent studies have shown that the signalling functions of ROS, RNS and RCS, most particularly hydrogen peroxide, nitric oxide (NO) and methylglyoxal (MG), provide resistance to abiotic stresses and underpin cross-stress tolerance in plants by modulating the expression of genes as well as the post-translational modification of proteins. The current review highlights the key regulators and mechanisms underlying heat or cold priming-induced cross-stress tolerance in plants, with a focus on ROS, MG and NO signalling, as well as on the role of antioxidant and glyoxalase systems, osmolytes, heat-shock proteins (HSPs) and hormones. Our aim is also to provide a comprehensive idea on the topic for researchers using heat or cold priming-induced cross-tolerance as a mechanism to improve crop yields under multiple abiotic stresses.

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References

  • Ahmad R, Kim YH, Kim MD, Kwon SY, Cho K, Lee HS, Kwak SS (2010) Simultaneous expression of choline oxidase, superoxide dismutase and ascorbate peroxidase in potato plant chloroplasts provides synergistically enhanced protection against various abiotic stresses. Physiol Plant 138:520–533

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran LSP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

    PubMed  PubMed Central  Google Scholar 

  • Akram NA, Waseem M, Ameen R, Ashraf M (2016) Trehalose pretreatment induces drought tolerance in radish (Raphanus sativus L.) plants: some key physio-biochemical traits. Acta Physiol Plant 38:3

    Article  CAS  Google Scholar 

  • Alam MM, Nahar K, Hasanuzzaman M, Fujita M (2014) Exogenous jasmonic acid modulates the physiology, antioxidant defense and glyoxalase systems in imparting drought stress tolerance in different Brassica species. Plant Biotechnol Rep 8:279–293

    Article  Google Scholar 

  • Ali Q, Anwar F, Ashraf M, Saari N, Perveen R (2013) Ameliorating effects of exogenously applied proline on seed composition, seed oil quality and oil antioxidant activity of maize (Zea mays L.) under drought stress. Int J Mol Sci 14:818–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alonos A, Queiroz CS, Magalhaes AC (1997) Chilling stress leads to increased cell membrane rigidity in roots of coffee (Coffea arabica L.) seedlings. Biochim Biophys Acta 1323:75–84

    Article  Google Scholar 

  • Antoniou C, Savvides A, Christou A, Fotopoulos V (2016) Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr Opin Plant Biol 33:101–107

    Article  CAS  PubMed  Google Scholar 

  • Awasthi R, Bhandari K, Nayyar H (2015) Temperature stress and redox homeostasis in agricultural crops. Front Environ Sci 3:11

    Article  Google Scholar 

  • Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphlides C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13:519–527

    Article  CAS  PubMed  Google Scholar 

  • Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2012) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88

    Article  CAS  Google Scholar 

  • Bäurle I (2016) Plant heat adaptation: priming in response to heat stress. F1000Res 5(F1000 Faculty Rev): 694

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front Plant Sci 7:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Cantrel C, Vazquez T, Puyaubert J, Reze N, Lesch M, Kaiser WM, Dutilleul C, Guillas I, Zachowski A, Baudouin E (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol 189:415–427

    Article  CAS  PubMed  Google Scholar 

  • Cao F, Hua C, Cheng S, Li L, Xu F, Yu W, Yuan H (2012) Expression of selected Ginko biloba heat shock protein genes and cold treatment could be induced by other abiotic stress. Int J Mol Sci 13:5768–5788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao YY, Kao CH (2010) Heat shock-induced ascorbic acid accumulation in leaves increases cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 336:39–48

    Article  CAS  Google Scholar 

  • Chao YY, Hsu YT, Kao CH (2009) Involvement of glutathione in heat shock-and hydrogen peroxide-induced cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 318:37–45

    Article  CAS  Google Scholar 

  • Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  CAS  Google Scholar 

  • Cheng Z, Jin R, Cao M, Liu X, Chan Z (2016) Exogenous application of ABA mimic 1 (AM1) improves cold stress tolerance in bermudagrass (Cynodon dactylon). Plant Cell Tissue Organ Cult 125:231–240

    Article  CAS  Google Scholar 

  • Chou TS, Chao YY, Kao CH (2012) Involvement of hydrogen peroxide in heat shock- and cadmium-induced expression of ascorbate peroxidase and glutathione reductase in leaves of rice seedlings. J Plant Physiol 169:478–486

    Article  CAS  PubMed  Google Scholar 

  • Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxid Redox Signal 21:1305–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ (2016) Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2:e1501340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cruz FJR, Castro GLS, Silva Júnior DD, Festucci-Buselli RA, Pinheiro HA (2013) Exogenous glycine betaine modulates ascorbate peroxidase and catalase activities and prevent lipid peroxidation in mild water-stressed Carapa guianensis plants. Photosynthetica 51:102–108

    Article  CAS  Google Scholar 

  • dos Reis SP, Lima AM, de Souza CRB (2012) Recent molecular advances on downstream plant response to abiotic stress. Int J Mol Genet 13:8628–8647

    Google Scholar 

  • Driedonks N, Xu J, Peters JL, Park S, Rieu I (2015) Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. Front Plant Sci 6:999

    Article  PubMed  PubMed Central  Google Scholar 

  • Einset J, Connolly EL (2009) Glycine betaine enhances extracellular processes blocking ROS signaling during stress. Plant Signal Behav 4:197–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan W, Zhang M, Zhang H, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS One 7:e37344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faralli M, Lektemur C, Rosellini D, Gürel F (2015) Effects of heat shock on salinity tolerance in barley (Hordeum vulgare L.): plant growth and stress-related gene transcription. Biol Plant 59:537–546

    Article  CAS  Google Scholar 

  • Farnese FS, Oliveira JA, Paiva EAS, Menezes-Silva PE, da Silva AA, Campos FV, Ribeiro C (2017) The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front Plant Sci 8:516

    PubMed  PubMed Central  Google Scholar 

  • Ferreira-Silva SL, Voigt EL, Silva EN, Maia JM, Fontenele AV, Silveira JAG (2011) High temperature positively modulates oxidative protection in salt-stressed cashew plants. Environ Exp Bot 74:162–170

    Article  CAS  Google Scholar 

  • Fowler DB, N'Diaye A, Laudencia-Chingcuanco D, Pozniak CJ (2016) Quantitative trait loci associated with phenological development, low-temperature tolerance, grain quality, and agronomic characters in wheat (Triticum aestivum L.). PLoS ONE 11:e0152185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17:1233–1240

    Article  CAS  PubMed  Google Scholar 

  • Gong M, Chen B, Li ZG, Guo LH (2001) Heat-shock-induced cross adaptation to heat, chilling, drought and salt stress in maize seedlings and involvement of H2O2. J Plant Physiol 158:112–1130

    Article  Google Scholar 

  • Grigorova B, Vaseva II, Demirevska K, Feller U (2011) Expression of selected heat shock proteins after individually applied and combined drought and heat stress. Acta Physiol Plant 33:2041–2049

    Article  CAS  Google Scholar 

  • Grover A, Mittal D, Negi M, Lavania D (2013) Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci 205-206:38–47

    Article  CAS  PubMed  Google Scholar 

  • Guler NS, Pehlivan N (2016) Exogenous low-dose hydrogen peroxide enhances drought tolerance of soybean (Glycine max L.) through inducing antioxidant system. Acta Biol Hung 67:169–183

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH (2016) The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 7:114

    PubMed  PubMed Central  Google Scholar 

  • Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to sodium chloride: complex I is protected by anti-oxidants and small heat-shock proteins, while complex II is protected by proline and betaine. Plant Physiol 126:1266–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365

    Article  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2012) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323

    CAS  Google Scholar 

  • Heino P, Sandman G, Lhng V, Nordin K, Palva ET (1990) Abscisic acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 79:801–806

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Tuya A, Nakamura Y, Murata Y (2012a) Methylglyoxal inhibits seed germination and root elongation and up-regulates transcription of stress-responsive genes in ABA-dependent pathway in Arabidopis. Plant Biol 14:854–858

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Ye W, Hossain MA, Nakamura Y, Murata Y (2012b) Methylglyoxal-induced stomatal closure accompanied by peroxidase-mediated ROS production in Arabidopsis. J Plant Physiol 169:979–986

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran LSP (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341

    Article  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Fujita M (2009) Purification of glyoxalase I from onion bulbs and molecular cloning of its cDNA. Biosci Biotechnol Biochem 73:2007–2013

    Article  CAS  PubMed  Google Scholar 

  • Hossain MA, Fujita M (2013) Hydrogen peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.). Plant Gene Trait 4:109–123

    Google Scholar 

  • Hossain MA, Hossain MZ, Fujita M (2009) Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3:53–64

    CAS  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Teixeira da Silva JA, Fujita M (2011) Glyoxalase system and reactive oxygen species detoxification system in plant abiotic stress response and tolerance: an intimate relationship. In: Shanker A, Venkateswarlu B (eds) Abiotic stress in plants—mechanisms and adaptations. INTECH, Rijeka, pp 235–266

    Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013a) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70

    Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013b) Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings. J Plant Sci Mol Breed 2:1–14

    Article  CAS  Google Scholar 

  • Hossain MA, Mostofa MG, Burritt DJ, Fujita M (2014) Modulation of reactive oxygen species and methylglyoxal detoxification systems by exogenous glycinebetaine and proline improves drought tolerance in mustard (Brassica juncea L.). Int J Plant Biol Res 2:1014

    Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Burritt DJ, Fujita M (2016a) Cross-stress tolerance in plants: molecular mechanisms and possible involvement of reactive oxygen species and methylglyoxal detoxification systems. In: Tuteja N, Gill SS (eds) Abiotic stress response in Plants. Wiley, Weinheim, pp 323–376

    Google Scholar 

  • Hossain MA, Burritt DJ, Fujita M (2016b) Proline and glycine betaine modulate cadmium-induced oxidative stress tolerance in plants: possible biochemical and molecular mechanisms. In: Azooz MM, Ahmad P (eds) Plant-environment interaction: responses and approaches to mitigate stress. Wiley, Chichester, pp 97–123

    Google Scholar 

  • Hsu YT, Kao CH (2007) Heat shock-mediated H2O2 accumulation and protection against cd toxicity in rice seedlings. Plant Soil 300:137–147

    Article  CAS  Google Scholar 

  • Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Li Y, Li C, Yang H, Wang W, Lu M (2010) Characterization of small heat shock proteins associated with maize tolerance to combined drought and heat stress. J Plant Growth Regul 29:455–464

    Article  CAS  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huner NPA, Oquist G, Hurry VM, Krol M, Kalk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39

    Article  CAS  PubMed  Google Scholar 

  • Hussain M, Malik MA, Farooq M, Ashraf MY, Cheema MA (2008) Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J Agro Crop Sci 194:193–199

    Article  CAS  Google Scholar 

  • Jacob P, Hirt H, Bendahmane A (2016) The heat shock protein/chaperone network and multiple stress resistance. Plant Biotech. doi:10.1111/pbi.12659

  • Jagadish SVK, Murty MVR, Quick WP (2014) Rice responses to rising temperatures-challenges, perspectives and future directions. Plant Cell Environ 38:1686–1698

    Article  PubMed  Google Scholar 

  • Jan N, Hossain MU, Andrabi KI (2009) Cold resistance in plants: a mystery unresolved. Electron J Biotechnol 12:1–15

    Article  Google Scholar 

  • Janská A, Marsík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation-what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  PubMed  CAS  Google Scholar 

  • Jaya N, Garcia V, Vierling E (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci U S A 106:15604–15609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin SH, Li XQ, Wang GG, Zhu XT (2015) Brassinosteroids alleviate high-temperature injury in Ficus concinna seedlings via maintaining higher antioxidant defence and glyoxalase systems. AoB Plants 7:plv009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • John R, Anjum NA, Sopory SK, Akram NA, Ashraf M (2016) Some key physiological and molecular processes of cold acclimation. Biol Plant 60(4):603-618. doi:10.1007/s10535-016-0648-9

  • Kang HM, Saltveit ME (2001) Activity of enzymatic antioxidant defense systems in chilled and heat shocked cucumber seedling radicles. Physiol Plant 113:548–556

    Article  CAS  Google Scholar 

  • Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur C, Ghosh A, Pareek A, Sopory SK, Singla-Pareek SL (2014a) Glyoxalases and stress tolerance in plants. Biochem Soc Trans 42:485–490

    Article  CAS  PubMed  Google Scholar 

  • Kaur C, Singla-Pareek SL, Sopory SK (2014b) Glyoxalase and methylglyoxal as biomarkers for plant stress tolerance. Crit Rev Plant Sci 33:429–456

    Article  CAS  Google Scholar 

  • Kaur C, Kushwaha HR, Mustafiz A, Pareek A, Sopory SK, Singla-Pareek SL (2015) Analysis of global gene expression profile of rice in response to methylglyoxal indicates its possible role as a stress signal molecule. Front Plant Sci 6:682

    PubMed  PubMed Central  Google Scholar 

  • Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiol Mol Biol Plants 17:203–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MS, Ahmad D, Khan MA (2015) Utilization of genes encoding osmoprotectants in transgenic plants for enhanced abiotic stress tolerance. Electron J Biotechnol 18:257–266

    Article  CAS  Google Scholar 

  • Kishitani S, Watanabe K, Yasuda S, Arakawa K, Takabe T (1994) Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ 17:89–95

    Article  CAS  Google Scholar 

  • Kissoudis C, van de Wiel C, Visser RGF, van der Linden G (2014) Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Front Plant Sci 5:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Kissoudis C, Sunarti S, van de Wiel C, Visser RGF, van der Linden CG, Bai Y (2016) Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism. J Exp Bot 67:5119–5132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Prášil IT, Vítámvás P, Dobrev P, Motyka V, Floková K, Novák O, Turečková V, Rolčik J, Pešek B, Trávničková A, Gaudinová A, Galiba G, Janda T, Vlasáková E, Prásilová P, Vanková R (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsov VV, Rakitin VY, Borisova NN, Rotschupkin BV (1993) Why does heat shock increase salt resistance in cotton plants? Plant Physiol Biochem 31:181–188

    CAS  Google Scholar 

  • Kuznetsov VV, Rakitin VY, Zholkevich VN (1999) Effect of preliminary heat-shock treatment on accumulation of osmolytes and drought resistance in cotton plants during water deficiency. Physiol Plant 107:399–406

    Article  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161:405–413

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KW, Cha JY, Kim KH, Kim YG, Lee BH, Lee SH (2012) Overexpression of alfalfa mitochondrial HSP23 in prokaryotic and eukaryotic model systems confers enhanced tolerance to salinity and arsenic stress. Biotechnol Lett 34:167–174

    Article  CAS  PubMed  Google Scholar 

  • Lei YB, Song SQ, Fu JR (2005) Possible involvement of antioxidant enzymes in the cross-tolerance of the germination/growth of wheat seeds to salinity and heat stress. J Integr Plant Biol 47:1211–1219

    Article  CAS  Google Scholar 

  • Li ZG (2016) Methylglyoxal and glyoxalase system in plants: old players, new concepts. Bot Rev 82:183–203

    Article  Google Scholar 

  • Li ZG, Gong M (2011) Mechanical stimulation-induced cross-adaptation in plants: an overview. J Plant Biol 54:358–364

    Article  Google Scholar 

  • Li HW, Zang BS, Deng XW, Wang XP (2011) Overexpression of the trehalose-6- phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018

    Article  CAS  PubMed  Google Scholar 

  • Li M, Ji L, Yang X, Meng Q, Guo S (2012) The protective mechanisms of CaHSP26 in transgenic tobacco to alleviate photoinhibition of PSII during chilling stress. Plant Cell Rep 31:1969–1979

    Article  CAS  PubMed  Google Scholar 

  • Li SL, Xia YZ, Liu J (2014) Effects of cold-shock on tomato seedlings under high-temperature stress. Chin J Appl Ecol 25:2927–2934

    CAS  Google Scholar 

  • Li X, Topbjerg HB, Jiang D, Liu F (2015) Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage. Plant Soil 393:307–318

    Article  CAS  Google Scholar 

  • Li ZG, Duan XQ, Xia YM, Wang Y, Zhou ZH, Min X (2016a) Methylglyoxal alleviates cadmium toxicity in wheat (Triticum aestivum L). Plant Cell Rep. doi:10.1007/s00299-016-2070-3

  • Li ZG, Min X, Zhou Z (2016b) Hydrogen sulfide: a signal molecule in plant cross-adaptation. Front Plant Sci 7:162

    Article  CAS  Google Scholar 

  • Li ZG, Duan XQ, Min X, Zhou ZH (2017) Methylglyoxal as a novel signal molecule induces the salt tolerance of wheat by regulating the glyoxalase system, the antioxidant system, and osmolytes. Protoplasma. doi:10.1007/s00709-017-1094-z

  • Liu HT, Liu YY, Pan QH, Yang HR, Zhang JC, Huang WD (2006) Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347

    Article  CAS  PubMed  Google Scholar 

  • Liu D, He S, Zhai H, Wang L, Zhao Y, Wang B et al (2014) Overexpression of IbP5CR enhances salt tolerance in transgenic sweet potato. Plant Cell Tiss Organ Cult 117:1–16

    Article  CAS  Google Scholar 

  • Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y et al (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.) BMC Plant Biol 15:152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Masand S, Yadav SK (2016) Overexpression of MuHSP70 gene from Macrotyloma uniflorum confers multiple abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep 43:53–64

    Article  CAS  PubMed  Google Scholar 

  • Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485

    Article  CAS  PubMed  Google Scholar 

  • McClung CR, Davis SJ (2010) Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol 20:R1086–R1092

    Article  CAS  PubMed  Google Scholar 

  • Mei YQ, Song SQ (2010) Response to temperature stress of reactive oxygen species scavenging enzymes in the cross-tolerance of barley seed germination. J Zhejiang Univ Sci B 11:965–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meissner M, Orsini E, Ruschhaupt M, Melchinger AE, Hincha DK, Heyer AG (2013) Mapping quantitative trait loci for freezing tolerance in a recombinant inbred line population of Arabidopsis thaliana accessions Tenela and C24 reveals REVEILLE1 as negative regulator of cold acclimation. Plant Cell Environ 36:1256–1267

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2016) ROS are good. Trends Plant Sci. doi:10.1016/j.Tplants.2016.08.002

  • Mittler R, Frinka A, Goloubinoff P (2012) How do plants feel the heat? Trends Plant Sci 37:118–125

    CAS  Google Scholar 

  • Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Yoshida N, Fujita M (2014) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul 73:31–44

    Article  CAS  Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M, Tran LS (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mu C, Zhang S, Yu G, Chen N, Li X, Liu H (2013) Overexpression of small heat shock protein LimHSP16.45 in Arabidopsis enhances tolerance to abiotic stresses. PLoS One 8:e82264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mudalkar S, Shrrharsha RV, Reddy AR (2017) Involvement of glyoxalases and glutathione reductase in conferring abiotic stress tolerance to Jatropha curcas L. Environ Exp Bot 134:141–150

    Article  CAS  Google Scholar 

  • Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19

    Article  PubMed  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54

    Article  CAS  Google Scholar 

  • Nayyar H, Bains TS, Kumar S (2005) Chilling stressed chickpea seedlings: effect of cold acclimation, calcium and abscisic acid on cryoprotective solutes and oxidative damage. Environ Exp Bot 54:275–285

    Article  CAS  Google Scholar 

  • Nollen EA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci 115:2809–2816

    CAS  PubMed  Google Scholar 

  • Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:596–604

    Article  CAS  PubMed  Google Scholar 

  • Pandey P, Ramegowda V, Senthil-Kumar M (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:723

    Article  PubMed  PubMed Central  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:1–6

    Article  CAS  Google Scholar 

  • Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628

  • Peng J, Li Z, Wen X, Li W, Shi H, Yang L et al (2014) Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genet 10:e1004664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pereira A (2016) Plant abiotic stress challenges from the changing environment. Front Plant Sci 7:1123

    PubMed  PubMed Central  Google Scholar 

  • Perez IB, Brown PJ (2014) The role of ROS signaling in cross-tolerance: from model to crop. Front Plant Sci 5:754

    Article  PubMed  PubMed Central  Google Scholar 

  • Pompeiano A, Vita F, Miele S, Guglielminetti L (2013) Freeze tolerance and physiological changes during cold acclimation of giant reed (Arundo donax L.). Grass Forage Sci 70:168–175

    Article  Google Scholar 

  • Puniran-Hartley N, Hartley J, Shabala L, Shabala S (2014) Salinity-induced accumulation of organic osmolytes in barley and wheat leaves correlates with increased oxidative stress tolerance: in planta evidence for cross-tolerance. Plant Physiol Biochem 83:32–39

    Article  CAS  PubMed  Google Scholar 

  • Puyaubert J, Baudouin E (2014) New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ 37:2623–2630

    Article  CAS  PubMed  Google Scholar 

  • Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208

    Article  CAS  PubMed  Google Scholar 

  • Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    Article  CAS  PubMed  Google Scholar 

  • Rabbani N, Thornalley PJ (2012) Methylglyoxal, glyoxalase 1 and the dicarbonyl proteome. Amino Acids 42:1133–1142

    Article  CAS  PubMed  Google Scholar 

  • Rejeb IB, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3:458–475

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Renaut J, Hoffmann L, Hausman JF (2005) Biochemical and physiological mechanisms related to cold acclimation and enhanced freezing tolerance in poplar plantlets. Physiol Plant 125:82–94

    Article  CAS  Google Scholar 

  • Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rihan HZ, Al-Issawi M, Fuller MP (2017) Advances in physiological and molecular aspects of plant cold tolerance. J Plant Interact 12(1):143–157

    Article  Google Scholar 

  • Saito R, Yamamoto H, Makino A, Sugimoto T, Miyake C (2011) Methylglyoxal functions as hill oxidant and stimulates the photoreduction of O2 at photosystem I: a symptom of plant diabetes. Plant Cell Environ 34:1454–1464

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Imai R (2012) Pleiotropic roles of cold shock domain proteins in plants. Front Plant Sci 2:116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sato Y, Murakami T, Funatsuki H, Matsuba S, Saruyama H, Tanida M (2001) Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings. J Exp Bot 52:145–151

    Article  CAS  PubMed  Google Scholar 

  • Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci 21:329–340

    Article  CAS  PubMed  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:187

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi H, Chen L, Ye T, Liu X, Ding K, Chan Z (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Biochem 82:209–217

    Article  CAS  PubMed  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song L, Jiang Y, Zhao H, Hou M (2012) Acquired thermotolerance in plants. Plant Cell Tissue Organ Cult 111:265–276

    Article  CAS  Google Scholar 

  • Song A, Zhu X, Chen F, Gao H, Jiang J, Chen SA (2014) Chrysanthemum heat shock protein confers tolerance to abiotic stress. Int J Mol Sci 15:5063–5078

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Streb P, Aubert S, Gout E, Feierabend J, Bligny R (2008) Cross tolerance to heavy-metal and cold-induced photoinhibition in leaves of Pisum sativum acclimated to low temperature. Physiol Mol Biol Plants 14:185–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler S, Miller G (2012) ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D et al (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One 11:e0147625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Szarka A, Tomasskovics B, Bánhegyi G (2012) The ascorbate-glutathione- α-tocopherol triad in abiotic stress response. Int J Mol Sci 13:4458–4483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur P, Nayyar H (2013) Facing the cold stress by plants in the changing environment: sensing, signaling and defending mechanisms. In: Tuteja N, Gill S (eds) Plant acclimation to environmental stress. Springer, New York, pp 29–69

    Chapter  Google Scholar 

  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock protein (HSP). J Proteome Res 71:391–411

    Article  CAS  Google Scholar 

  • Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol 29:57–63

    Article  CAS  PubMed  Google Scholar 

  • Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523

    Article  CAS  Google Scholar 

  • Upadhyaya CP, Venkatesh J, Gururani MA, Asnin L, Sharma K, Ajappala H et al (2011) Transgenic potato overproducing L-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol Lett 33:2297–2307

    Article  CAS  PubMed  Google Scholar 

  • Vanková R, Kosová K, Dobrev P, Vítámvás P, Trávníčková A, Cvikrová M, Pesek B, Gaudinová A, Prerostová S, Musilová J, Galiba G, Prásil IT (2014) Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level. Environ Exp Bot 101:12–25

    Article  CAS  Google Scholar 

  • Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant–environment interaction. Arabidopsis book 8:e0140

    Article  PubMed  PubMed Central  Google Scholar 

  • Verslues PE, Zhu J (2004) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379

    Article  Google Scholar 

  • Walter J, Jentsch A, Beierkuhnlein C, Kreyling J (2013) Ecological stress memory and cross stress tolerance in plants in the fact of climate extremes. Environ Exp Bot 94:3–8

    Article  Google Scholar 

  • Wan SB, Tian L, Tian RR, Pan QH, Zhan JC, Wen PF, Chen JY, Zhang P, Wang W, Huang WD (2009) Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiol Biochem 47:504–510

    Article  CAS  PubMed  Google Scholar 

  • Wan X, Yang J, Li X, Zhou Q, Guo C, Bao M et al (2016) Over-expression of PmHSP17.9 in transgenic Arabidopsis thaliana confers thermotolerance. Plant Mol Biol Rep 34:899–908

    Article  CAS  Google Scholar 

  • Wang AQ, Yu XH, Mao Y, Liu Y, Liu GQ, Liu YS et al (2015) Overexpression of a small heat-shock-protein gene enhances tolerance to abiotic stresses in rice. Plant Breed 134:384–393

    Article  CAS  Google Scholar 

  • Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176

    Article  Google Scholar 

  • Welchen E, Schmitz J, Fuchs P, García L, Wagner S, Wienstroer J et al (2016) D-lactate dehydrogenase links methylglyoxal degradation and electron transport through cytochrome C. Plant Physiol 172:901–912

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol 8:749–771

    Article  CAS  Google Scholar 

  • Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856

    Article  CAS  PubMed  Google Scholar 

  • Xin Z, Browse J (1998) eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci U S A 95:7799–7804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing W, Rajashekar CB (2001) Glycinebetaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 46:21–28

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Zhang M, Zhang X, Han LB (2015) Cold acclimation treatment-induced changes in abscisic acid, cytokinin, and antioxidant metabolism in Zoysiagrass (Zoysia japonica). Hort Sci 50:107–1080

    Google Scholar 

  • Xuan Y, Zhou S, Wang L, Cheng Y, Zhao L (2010) Nitric oxide functions as a signal and acts upstream of atcam3 in thermotolerance in Arabidopsis seedlings. Plant Physiol 153:1895–1906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67

    Article  CAS  PubMed  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005b) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto CJT, Leite RGF, Minamiguchi JY, Braga I, Machado Neto NB, Custódio CC (2014) Water-deficit tolerance induction during germination of JaloPrecoce bean (Phaseolus vulgaris L.) cultivar. Acta Physiol Plant 36:2897–2904

    Article  Google Scholar 

  • Zandalinas SI, Balfagón D, Arbona V, Gómez-Cadenas A, Inupakutika MA, Mittler R (2016) ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress. J Exp Bot 67:5381–5390

  • Zhang X, Shen L, Li F, Meng D, Sheng J (2013) Arginase induction by heat treatment contributes to amelioration of chilling injury and activation of antioxidant enzymes in tomato fruit. Postharvest Biol Tech 79:1–8

    Article  CAS  Google Scholar 

  • Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Wang J, Shi K, Xia XJ, Zhou YH, Yu JQ (2012a) Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol Biochem 60:141–149

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Chen H, Chu P, Li Y, Tan B, Ding Y, Tsang EW, Jiang L, Wu K, Huang S (2012b) NnHSP17.5, a cytosolic class II small heat shock protein gene from Nelumbo nucifera, contributes to seed germination vigor and seedling thermotolerance in transgenic Arabidopsis. Plant Cell Rep 31:379–389

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Xia XJ, Zhou YH, Shi K, Chen Z, Yu JQ (2014) RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. J Exp Bot 65:595–607

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2016) Abiotic stress signalling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou J, Liu C, Liu A, Zou D, Chen X (2012) Overexpression of OsHsp17.0 and OsHsp23.7 enhances drought and salt tolerance in rice. J Plant Physiol 169:628–635

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh

    Mohammad Anwar Hossain

  2. School of Life Sciences, Yunnan Normal University, Kunming, 650500, People’s Republic of China

    Zhong-Guang Li

  3. Department of Soil Science, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh

    Tahsina Sharmin Hoque

  4. Department of Botany, University of Otago, Dunedin, New Zealand

    David J. Burritt

  5. Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa University, Takamatsu, Japan

    Masayuki Fujita

  6. Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Spain

    Sergi Munné-Bosch

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  1. Mohammad Anwar Hossain
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  2. Zhong-Guang Li
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  3. Tahsina Sharmin Hoque
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MAH, ZGL and TSH conceived the idea. MAH, ZGL, TSH, DJB, MF and SMB wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Mohammad Anwar Hossain.

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Hossain, M.A., Li, ZG., Hoque, T.S. et al. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 255, 399–412 (2018). https://doi.org/10.1007/s00709-017-1150-8

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